Environmental decomposition of cuticular hydrocarbons generates a volatile pheromone that guides insect social behavior

Abstract

28Once emitted, semiochemicals are exposed to reactive environmental factors that may alter them, 29 thus disrupting chemical communication. Some species, however, might have adapted to detect 30 environmentally mediated breakdown products of their natural chemicals as semiochemicals. We 31 demonstrate that air, water vapor, and ultraviolet (UV) radiation break down unsaturated cuticular 32 hydrocarbons (CHCs) of Periplaneta americana (American cockroach), resulting in the emission of 33 volatile organic compounds (VOCs). In behavioral assays, nymphs strongly avoided aggregating in 34 shelters exposed to the breakdown VOCs from cuticular alkenes. The three treatments (air, water 35 vapor, UV) produced the same VOCs, but at different time-courses and ratios. Fourteen VOCs from 36 UV-exposed CHCs elicited electrophysiological responses in nymph antennae; 10 were identified as 37 1-pentanol, 1-octanol, 1-nonanol, tetradecanal, acetic acid, propanoic acid, butanoic acid, pentanoic 38 acid and hexanoic acid. When short-chain fatty acids were tested as a mix and a blend of the alcohols 39 and aldehyde was tested as a second mix, nymphs exhibited no preference for control or treated 40 shelters. However, nymphs avoided shelters that were exposed to VOCs from the complete 10-41 compound mix. Conditioned shelters (occupied by cockroaches with feces and CHCs deposited on the 42 shelters), which are normally highly attractive to nymphs, were also avoided after UV-exposure, 43 confirming that breakdown products from deposited metabolites, including CHCs, mediate this 44 behavior. Our results demonstrate that common environmental and anthropogenic agents degrade 45CHCs into volatile semiochemicals that may serve as necromones or epideictic pheromones, 46 mediating group formation and dissolution. 47 Significance Statement 53Cuticular hydrocarbons (CHCs) cover the outer surface of insects, where they prevent water 54 loss and serve as sex pheromones and in nest-mate recognition in social insects. Although CHCs are 55 not volatile, they can be broken into volatile fragments by reacting with environmental agents. We 56 demonstrate that volatile breakdown products of CHCs affect the social behavior of the American 57 cockroach. A synthetic mix of volatiles dispersed cockroaches away from shelters, signaling an 58 unsuitable shelter. These results highlight that some insect species have evolved communication 59 strategies that exploit environmental and anthropogenic agents to produce bioactive compounds 60 that mediate ecological interactions.

Chemical Ecology, Biochemistry, and Molecular Biology of Insect Hydrocarbons

“…Photo-oxidation of CHCs has also been implicated in the formation of volatile semiochemicals in a variety of other insect taxa including Macrocentrus grandii (103), Anoplophora glabripennis (112), and Drosophila melanogaster (71). Recently, Hatano et al (59) demonstrated that nymphs of the American cockroach, P. americana, avoided shelters exposed to volatiles originating from the breakdown of CHCs. In particular, exposing CHCs to ultraviolet radiation resulted in the release of 14 compounds detectable by the cockroach antennae, and a blend of 10 of them elicited avoidance behavior, suggesting that they serve as necromones (signals of death) or epideictic (spacing) pheromones.…”

Characterization of Dominant Cuticular Hydrocarbons in Inversion and Inversion-Free Strains of <i>Drosophila ananassae</i> (Doleschall)

“…CHCs are species-specific and serve multiple functions. The primary role of CHCs is protecting the insects from environmental stress and also evolved secondary functions as chemical signals (Hatano et al, 2019;Pardy et al, 2019). n-alkanes are majorly involved in desiccation resistance increasing the chain length strengthens van der Waals forces with high melting points leads to stability.…”